Dynamics of <i>cis</i>-regulatory sequences and transcriptional divergence of duplicated genes in soybean

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Significance

We analyzed the transcriptional regulation of 17,111 pairs of duplicated genes in soybean, which were derived from a whole genome duplication (WGD) that occurred about 5 to 13 Mya. We demonstrate that gain or loss of flanking regulatory sequences and mutation of cis-regulatory elements within the sequences can change the balance of the expression level and/or tissue specificity of duplicated genes. These results support our hypothesis that dynamics of the cis-regulatory sequences after the recent WGD event has played an important role in transcriptional divergence of duplicated genes in soybean, which may represent a general mechanism for divergence of duplicated genes in polyploids that lack subgenome dominance.

Abstract

Transcriptional divergence of duplicated genes after whole genome duplication (WGD) has been described in many plant lineages and is often associated with subgenome dominance, a genome-wide mechanism. However, it is unknown what underlies the transcriptional divergence of duplicated genes in polyploid species that lack subgenome dominance. Soybean is a paleotetraploid with a WGD that occurred 5 to 13 Mya. Approximately 50% of the duplicated genes retained from this WGD exhibit transcriptional divergence. We developed accessible chromatin region (ACR) datasets from leaf, flower, and seed tissues using MNase-hypersensitivity sequencing. We validated enhancer function of several ACRs associated with known genes using CRISPR/Cas9-mediated genome editing. The ACR datasets were used to examine and correlate the transcriptional patterns of 17,111 pairs of duplicated genes in different tissues. We demonstrate that ACR dynamics are correlated with divergence of both expression level and tissue specificity of individual gene pairs. Gain or loss of flanking ACRs and mutation of cis-regulatory elements (CREs) within the ACRs can change the balance of the expression level and/or tissue specificity of the duplicated genes. Analysis of DNA sequences associated with ACRs revealed that the extensive sequence rearrangement after the WGD reshaped the CRE landscape, which appears to play a key role in the transcriptional divergence of duplicated genes in soybean. This may represent a general mechanism for transcriptional divergence of duplicated genes in polyploids that lack subgenome dominance.

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FIMO: scanning for occurrences of a given motif

Charles Grant, Timothy L. Bailey, William Noble (2011)

Summary: A motif is a short DNA or protein sequence that contributes to the biological function of the sequence in which it resides. Over the past several decades, many computational methods have been described for identifying, characterizing and searching with sequence motifs. Critical to nearly any motif-based sequence analysis pipeline is the ability to scan a sequence database for occurrences of a given motif described by a position-specific frequency matrix. Results: We describe Find Individual Motif Occurrences (FIMO), a software tool for scanning DNA or protein sequences with motifs described as position-specific scoring matrices. The program computes a log-likelihood ratio score for each position in a given sequence database, uses established dynamic programming methods to convert this score to a P-value and then applies false discovery rate analysis to estimate a q-value for each position in the given sequence. FIMO provides output in a variety of formats, including HTML, XML and several Santa Cruz Genome Browser formats. The program is efficient, allowing for the scanning of DNA sequences at a rate of 3.5 Mb/s on a single CPU. Availability and Implementation: FIMO is part of the MEME Suite software toolkit. A web server and source code are available at http://meme.sdsc.edu. Contact: t.bailey@imb.uq.edu.au; t.bailey@imb.uq.edu.au Supplementary information: Supplementary data are available at Bioinformatics online.

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Rapid isolation of high molecular weight plant DNA.

M Murray, W. Thompson (1980)

A method is presented for the rapid isolation of high molecular weight plant DNA (50,000 base pairs or more in length) which is free of contaminants which interfere with complete digestion by restriction endonucleases. The procedure yields total cellular DNA (i.e. nuclear, chloroplast, and mitochondrial DNA). The technique is ideal for the rapid isolation of small amounts of DNA from many different species and is also useful for large scale isolations.

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Genome sequence of the palaeopolyploid soybean.

Jeremy Schmutz, Steven Cannon, Jessica Schlueter … (2010)

Soybean (Glycine max) is one of the most important crop plants for seed protein and oil content, and for its capacity to fix atmospheric nitrogen through symbioses with soil-borne microorganisms. We sequenced the 1.1-gigabase genome by a whole-genome shotgun approach and integrated it with physical and high-density genetic maps to create a chromosome-scale draft sequence assembly. We predict 46,430 protein-coding genes, 70% more than Arabidopsis and similar to the poplar genome which, like soybean, is an ancient polyploid (palaeopolyploid). About 78% of the predicted genes occur in chromosome ends, which comprise less than one-half of the genome but account for nearly all of the genetic recombination. Genome duplications occurred at approximately 59 and 13 million years ago, resulting in a highly duplicated genome with nearly 75% of the genes present in multiple copies. The two duplication events were followed by gene diversification and loss, and numerous chromosome rearrangements. An accurate soybean genome sequence will facilitate the identification of the genetic basis of many soybean traits, and accelerate the creation of improved soybean varieties.

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Author and article information

Contributors

Fanli Meng:

ORCID: https://orcid.org/0000-0002-0942-1798

Jiming Jiang

Journal

Journal ID (nlm-ta): Proc Natl Acad Sci U S A

Journal ID (iso-abbrev): Proc Natl Acad Sci U S A

Journal ID (publisher-id): PNAS

Title: Proceedings of the National Academy of Sciences of the United States of America

Publisher: National Academy of Sciences

ISSN (Print): 0027-8424

ISSN (Electronic): 1091-6490

Publication date (Electronic, pub): 23 October 2023

Publication date (Print, pub): 31 October 2023

Publication date PMC-release: 23 April 2024

Volume: 120

Issue: 44

Electronic Location Identifier: e2303836120

Affiliations

[1] ^aDepartment of Plant Biology, Michigan State University , East Lansing, MI 48824

[2] ^bNortheast Institute of Geography and Agroecology, Key Laboratory of Soybean Molecular Design Breeding, Chinese Academy of Sciences , Harbin 150081, China

[3] ^cKey Laboratory of Soybean Biology in Chinese Ministry of Education, Northeast Agricultural University , Harbin 150030, China

[4] ^dAgro-Biotechnology Research Institute, Jilin Academy of Agricultural Sciences , Changchun 130033, China

[5] ^eDepartment of Horticulture, Michigan State University , East Lansing, MI 48824

[6] ^fMichigan State University AgBioResearch , East Lansing, MI 48824